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Characterization of freshly retrieved preantral follicles using a low-invasive, mechanical isolation method extended to different ruminant species

Published online by Cambridge University Press:  17 July 2014

A. Langbeen ,
E.P.A. Jorssen ,
E. Fransen ,
A.P.A. Rodriguez ,
M. Chong García ,
J.L.M.R. Leroy  and
P.E.J. Bols
A. Langbeen*
Affiliation:
University of Antwerp, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, Laboratory of Veterinary Physiology and Biochemistry, Universiteitsplein 1, Gebouw U, B-2610 Wilrijk, Belgium.
E.P.A. Jorssen
Affiliation:
University of Antwerp, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, Laboratory of Veterinary Physiology and Biochemistry, Universiteitsplein 1, Gebouw U, B-2610 Wilrijk, Belgium.
E. Fransen
Affiliation:
StatUa Center for Statistics, University of Antwerp, Prinsstraat 13, B-2000 Antwerp, Belgium.
A.P.A. Rodriguez
Affiliation:
Research Center for Biotechnology Transfer and Innovation, Laboratory of Manipulation of Oocytes and Preantral Follicles, Veterinary Faculty, State University of Ceará, Av. Paranjana 1700, Campus do Itaperi, Fortaleza, 60740–903, CE, Brazil.
M. Chong García
Affiliation:
University of Antwerp, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, Laboratory of Veterinary Physiology and Biochemistry, Universiteitsplein 1, Gebouw U, B-2610 Wilrijk, Belgium. CIMAGT Centro de Investigaciones para el Mejoramiento Animal de la Ganaderia Tropical, Calle 101, No. 6401 entre 64 y 100, Loma de Tierra, Cotorro, Ciudad de la Habana, Cuba.
J.L.M.R. Leroy
Affiliation:
University of Antwerp, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, Laboratory of Veterinary Physiology and Biochemistry, Universiteitsplein 1, Gebouw U, B-2610 Wilrijk, Belgium.
P.E.J. Bols
Affiliation:
University of Antwerp, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, Laboratory of Veterinary Physiology and Biochemistry, Universiteitsplein 1, Gebouw U, B-2610 Wilrijk, Belgium.
*
All correspondence to: A. Langbeen. University of Antwerp, Faculty of Pharmaceutical, Biomedical and Veterinary Sciences, Laboratory of Veterinary Physiology and Biochemistry, Universiteitsplein 1, Gebouw U, B-2610 Wilrijk, Belgium. Tel: +32 3 265 23 98. Fax: +32 3 265 24 33. e-mail: [email protected]
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Summary

Due to the increased interest in preantral follicular physiology, non-invasive retrieval and morphological classification are crucial. Therefore, this study aimed: (1) to standardize a minimally invasive isolation protocol, applicable to three ruminant species; (2) to morphologically classify preantral follicles upon retrieval; and (3) to describe morphological features of freshly retrieved follicles compared with follicle characteristics using invasive methods. Bovine, caprine and ovine ovarian cortex strips were retrieved from slaughterhouse ovaries and dispersed. This suspension was filtered, centrifuged, re-suspended and transferred to a Petri dish, to which 0.025 mg/ml neutral red (NR) was added to assess the viability of the isolated follicles. Between 59 and 191 follicles per follicle class and per species were collected and classified by light microscopy, based on follicular cell morphology. Subsequently, follicle diameters were measured. The proposed isolation protocol was applicable to all three species and showed a significant, expected increase in diameter with developmental stage. With an average diameter of 37 ± 5 μm for primordial follicles, 47 ± 6.3 μm for primary follicles and 67.1 ± 13.1 μm for secondary follicles, no significant difference in diameter among the three species was observed. Bovine, caprine and ovine follicles (63, 59 and 50% respectively) were graded as viable upon retrieval. Using the same morphological characteristics as determined by invasive techniques [e.g. haematoxylin–eosin (HE) sections], cumulus cell morphology and follicle diameter could be used routinely to classify freshly retrieved follicles. Finally, we applied a mechanical, minimally invasive, follicle isolation protocol and extended it to three ruminant species, yielding viable preantral follicles without compromising further in vitro processing and allowing routine follicle characterization upon retrieval.

Keywords

Follicle classificationLow-invasive follicle isolationMorphological characterizationPreantral folliclesRuminant reproduction
Type
Research Article
Information
Zygote , Volume 23 , Issue 5 , October 2015 , pp. 683 - 694
Copyright
Copyright © Cambridge University Press 2014 

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References

Abir, R., Roizman, P., Fisch, B., Nitke, S., Okon, E., Orvieto, R. & Ben Rafael, Z. (1999). Pilot study of isolated early human follicles cultured in collagen gels for 24 hours. Hum. Reprod. 14, 1299–301.CrossRefGoogle ScholarPubMed
Abir, R., Fisch, B., Nitke, S., Okon, E., Raz, A. & Ben Rafael, Z. (2001). Morphological study of fully and partially isolated early human follicles. Fertil. Steril. 75, 141–6.CrossRefGoogle ScholarPubMed
Abir, R., Nitke, S., Ben-Haroush, A. & Fisch, B. (2006). In vitro maturation of human primordial ovarian follicles: clinical significance, progress in mammals, and methods for growth evaluation. Histol. Histopathol. 21, 887–98.Google ScholarPubMed
Aerts, J.M. & Bols, P.E. (2010). Ovarian follicular dynamics: a review with emphasis on the bovine species. Part I: Folliculogenesis and pre-antral follicle development. Reprod. Domest. Anim. 45, 171–9.CrossRefGoogle ScholarPubMed
Aerts, J.M., De Clercq, J.B., Andries, S., Leroy, J.L., Van Aelst, S. & Bols, P.E. (2008a). Follicle survival and growth to antral stages in short-term murine ovarian cortical transplants after cryologic solid surface vitrification or slow-rate freezing. Cryobiology 57, 163–9.CrossRefGoogle ScholarPubMed
Aerts, J.M., Martinez-Madrid, B., Flothmann, K., De Clercq, J.B., Van Aelst, S. & Bols, P.E. (2008b). Quantification and viability assessment of isolated bovine primordial and primary ovarian follicles retrieved through a standardized biopsy pick-up procedure. Reprod. Domest. Anim. 43, 360–6.CrossRefGoogle ScholarPubMed
Aerts, J.M., Martinez-Madrid, B., Leroy, J.L., Van Aelst, S. & Bols, P.E. (2010). Xenotransplantation by injection of a suspension of isolated preantral ovarian follicles and stroma cells under the kidney capsule of nude mice. Fertil. Steril. 94, 708–14.CrossRefGoogle ScholarPubMed
Amorim, C.A., Rodrigues, A.P., Lucci, C.M., Figueiredo, J.R. & Goncalves, P.B. (2000). Effect of sectioning on the number of isolated ovine preantral follicles. Small Rumin. Res. 37, 269–77.CrossRefGoogle ScholarPubMed
Braw-Tal, R. (2002). The initiation of follicle growth: the oocyte or the somatic cells? Mol. Cell. Endocrinol. 187, 11–8.CrossRefGoogle ScholarPubMed
Braw-Tal, R. & Yossefi, S. (1997). Studies in vivo and in vitro on the initiation of follicle growth in the bovine ovary. J. Reprod. Fertil. 109, 165–71.CrossRefGoogle ScholarPubMed
Bukovsky, A., Caudle, M. R., Svetlikova, M., Wimalasena, J., Ayala, M.E. & Dominguez, R. (2005). Oogenesis in adult mammals, including humans: a review. Endocrine 26, 301–6.CrossRefGoogle ScholarPubMed
Campbell, B.K., Souza, C., Gong, J., Webb, R., Kendall, N., Marsters, P., Robinson, G., Mitchell, A., Telfer, E.E. & Baird, D.T. (2003). Domestic ruminants as models for the elucidation of the mechanisms controlling ovarian follicle development in humans. Reprod. Suppl. 61, 429–43.Google ScholarPubMed
Carambula, S.F., Goncalves, P.B., Costa, L.F., Figueiredo, J.R., Wheeler, M.B., Neves, J.P. & Mondadori, R.G. (1999). Effect of fetal age and method of recovery on isolation of preantral follicles from bovine ovaries. Theriogenology 52, 563–71.CrossRefGoogle ScholarPubMed
Cecconi, S., Barboni, B., Coccia, M. & Mattioli, M. (1999). In vitro development of sheep preantral follicles. Biol. Reprod. 60, 594–601.CrossRefGoogle ScholarPubMed
Chambers, E.L., Gosden, R.G., Yap, C. & Picton, H.M. (2010). In situ identification of follicles in ovarian cortex as a tool for quantifying follicle density, viability and developmental potential in strategies to preserve female fertility. Hum. Reprod. 25, 2559–68.CrossRefGoogle ScholarPubMed
Demeestere, I., Delbaere, A., Gervy, C., Van Den Bergh, M., Devreker, F. & Englert, Y. (2002). Effect of preantral follicle isolation technique on in-vitro follicular growth, oocyte maturation and embryo development in mice. Hum. Reprod. 17, 2152–9.CrossRefGoogle ScholarPubMed
Dolmans, M.M., Michaux, N., Camboni, A., Martinez-Madrid, B., Van Langendonckt, A., Nottola, S.A. & Donnez, J. (2006). Evaluation of Liberase, a purified enzyme blend, for the isolation of human primordial and primary ovarian follicles. Hum. Reprod. 21, 413–20.CrossRefGoogle ScholarPubMed
Donnez, J., Dolmans, M.M., Demylle, D., Jadoul, P., Pirard, C., Squifflet, J., Martinez-Madrid, B. & van Langendonckt, A. (2004). Livebirth after orthotopic transplantation of cryopreserved ovarian tissue. Lancet 364, 1405–10.CrossRefGoogle ScholarPubMed
Durrant, B.S., Pratt, N.C., Russ, K.D. & Bolamba, D. (1998). Isolation and characterization of canine advanced preantral and early antral follicles. Theriogenology 49, 917–32.CrossRefGoogle ScholarPubMed
Elliott, W.M. & Auersperg, N. (1993). Comparison of the neutral red and methylene blue assays to study cell growth in culture. Biotech. Histochem. 68, 29–35.CrossRefGoogle ScholarPubMed
Eppig, J.J. & O’Brien, M.J. (1996). Development in vitro of mouse oocytes from primordial follicles. Biol. Reprod., 54, 197–207.CrossRefGoogle ScholarPubMed
Fabbri, R., Pasquinelli, G., Keane, D., Mozzanega, B., Magnani, V., Tamburini, F. & Venturoli, S. (2009). Culture of cryopreserved ovarian tissue: state of the art in 2008. Fertil. Steril. 91, 1619–29.CrossRefGoogle ScholarPubMed
Fair, T. (2003). Follicular oocyte growth and acquisition of developmental competence. Anim. Reprod. Sci. 78, 203–16.CrossRefGoogle ScholarPubMed
Fair, T., Hulshof, S.C., Hyttel, P., Greve, T. & Boland, M. (1997). Oocyte ultrastructure in bovine primordial to early tertiary follicles. Anat. Embryol. 195, 327–36.CrossRefGoogle ScholarPubMed
Figueiredo, J.R., Hulshof, S.C., Van den Hurk, R., Ectors, F.J., Fontes, R.S., Nusgens, B., Bevers, M.M. & Beckers, J.F. (1993). Development of a combined new mechanical and enzymatic method for the isolation of intact preantral follicles from fetal, calf and adult bovine ovaries. Theriogenology 40, 789–99.CrossRefGoogle ScholarPubMed
Figueiredo, J.R., Hulshof, S.C., Van den Hurk, R., Nusgens, B., Bevers, M.M., Ectors, F.J. & Beckers, J.F. (1994). Preservation of oocyte and granulosa cell morphology in bovine preantral follicles cultured in vitro. Theriogenology 41, 1333–46.CrossRefGoogle ScholarPubMed
Figueiredo, J.R., Rodrigues, A.P., Silva, J.R. & Santos, R.R. (2011). Cryopreservation and in vitro culture of caprine preantral follicles. Reprod. Fertil. Dev. 23, 40–7.CrossRefGoogle ScholarPubMed
Fortune, J.E. (2003). The early stages of follicular development: activation of primordial follicles and growth of preantral follicles. Anim. Reprod. Sci. 78, 135–63.CrossRefGoogle ScholarPubMed
Fotakis, G. & Timbrell, J.A. (2006). In vitro cytotoxicity assays: comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride. Toxicol. Lett. 160, 171–7.CrossRefGoogle ScholarPubMed
Greenwald, G.S. & Moor, R.M. (1989). Isolation and preliminary characterization of pig primordial follicles. J. Reprod. Fertil. 87, 561–71.CrossRefGoogle ScholarPubMed
Gupta, P.S., Nandi, S., Ravindranatha, B.M. & Sarma, P.V. (2001). Isolation of preantral follicles from buffalo ovaries. Vet. Rec. 148, 543–4.CrossRefGoogle ScholarPubMed
Haag, K.T., Magalhaes-Padilha, D.M., Fonseca, G.R., Wischral, A., Gastal, M.O., King, S.S., Jones, K.L., Figueiredo, J.R. & Gastal, E.L. (2013). Equine preantral follicles obtained via the biopsy pick-up method: histological evaluation and validation of a mechanical isolation technique. Theriogenology 79, 735–43.CrossRefGoogle ScholarPubMed
Hazeleger, N.L., Hill, D.J., Stubbing, R.B. & Walton, J.S. (1995). Relationship of morphology and follicular fluid environment of bovine oocytes to their developmental potential in vitro. Theriogenology 43, 509–22.CrossRefGoogle ScholarPubMed
Hovatta, O., Wright, C., Krausz, T., Hardy, K. & Winston, R.M. (1999). Human primordial, primary and secondary ovarian follicles in long-term culture: effect of partial isolation. Hum. Reprod. 14, 2519–24.CrossRefGoogle ScholarPubMed
Hulshof, S.C., Figueiredo, J.R., Beckers, J.F., Bevers, M.M. & van den Hurk, R. (1994). Isolation and characterization of preantral follicles from foetal bovine ovaries. Vet. Q. 16, 78–80.CrossRefGoogle ScholarPubMed
Itoh, T. & Hoshi, H. (2000). Efficient isolation and long-term viability of bovine small preantral follicles in vitro. In Vitro Cell. Dev. Biol. 36, 235–40.2.0.CO;2>CrossRefGoogle ScholarPubMed
Johnson, J., Canning, J., Kaneko, T., Pru, J.K. & Tilly, J.L. (2004). Germline stem cells and follicular renewal in the postnatal mammalian ovary. Nature 428, 145–50.CrossRefGoogle ScholarPubMed
Kerr, J.B., Duckett, R., Myers, M., Britt, K.L., Mladenovska, T. & Findlay, J.K. (2006). Quantification of healthy follicles in the neonatal and adult mouse ovary: evidence for maintenance of primordial follicle supply. Reproduction 132, 95–109.CrossRefGoogle ScholarPubMed
Lee, D.M., Yeoman, R.R., Battaglia, D.E., Stouffer, R.L., Zelinski-Wooten, M.B., Fanton, J.W. & Wolf, D.P. (2004). Live birth after ovarian tissue transplant. Nature 428, 137–8.CrossRefGoogle ScholarPubMed
Lindner, G.M. & Wright, R.W. Jr. (1983). Bovine embryo morphology and evaluation. Theriogenology 20, 407–16.CrossRefGoogle ScholarPubMed
Lucci, C.M., Amorim, C.A., Bao, S.N., Figueiredo, J.R., Rodrigues, A.P., Silva, J.R. & Goncalves, P.B. (1999a). Effect of the interval of serial sections of ovarian tissue in the tissue chopper on the number of isolated caprine preantral follicles. Anim. Reprod. Sci. 56, 39–49.CrossRefGoogle ScholarPubMed
Lucci, C.M., Amorim, C.A., Rodrigues, A.P., Figueiredo, J.R., Bao, S.N., Silva, J.R. & Goncalves, P.B. (1999b). Study of preantral follicle population in situ and after mechanical isolation from caprine ovaries at different reproductive stages. Anim. Reprod. Sci. 56, 223–36.CrossRefGoogle ScholarPubMed
Lucci, C.M., Rumpf, R., Figueiredo, J.R. & Bao, S.N. (2002). Zebu (Bos indicus) ovarian preantral follicles: morphological characterization and development of an efficient isolation method. Theriogenology 57, 1467–83.CrossRefGoogle ScholarPubMed
Lucci, C.M., Silva, R.V., Carvalho, C.A., Figueiredo, R. & Bao, N. (2001). Light microscopical and ultrastructural characterization of goat preantral follicles. Small Rumin. Res. 41, 61–9.CrossRefGoogle ScholarPubMed
Lundy, T., Smith, P., O’Connell, A., Hudson, N.L. & McNatty, K.P. (1999). Populations of granulosa cells in small follicles of the sheep ovary. J. Reprod. Fertil. 115, 251–62.CrossRefGoogle ScholarPubMed
Malhi, P.S., Adams, G.P. & Singh, J. (2005). Bovine model for the study of reproductive aging in women: follicular, luteal, and endocrine characteristics. Biol. Reprod., 73, 45–53.CrossRefGoogle Scholar
Mandl, A.M. & Zuckerman, S. (1952). The growth of the oocyte and follicle in the adult rat. J. Endocrinol. 8, 126–32.CrossRefGoogle ScholarPubMed
Mayes, M.A. & Sirard, M.A. (2001). The influence of cumulus–oocyte complex morphology and meiotic inhibitors on the kinetics of nuclear maturation in cattle. Theriogenology 55, 911–22.CrossRefGoogle ScholarPubMed
Nayudu, P.L., Fehrenbach, A., Kiesel, P., Vitt, U. A., Pancharatna, K. & Osborn, S. (2001). Progress toward understanding follicle development in vitro: appearances are not deceiving. Arch. Med. Res. 32, 587–94.CrossRefGoogle Scholar
Nottola, S.A., Cecconi, S., Bianchi, S., Motta, C., Rossi, G., Continenza, M.A. & Macchiarelli, G. (2011). Ultrastructure of isolated mouse ovarian follicles cultured in vitro. Reprod. Biol. Endocrinol. 9, 3.CrossRefGoogle ScholarPubMed
Oktem, O. & Urman, B. (2010). Understanding follicle growth in vivo. Hum. Reprod. 25, 2944–54.CrossRefGoogle ScholarPubMed
Park, K.S., Lee, T.H., Park, Y.K., Song, H.B. & Chun, S.S. (2005). Effects of isolating methods (mechanical or enzymatical) on structure of pre-antral follicles in mouse. J. Assist. Reprod. Genet. 22, 355–9.CrossRefGoogle Scholar
Pedersen, T. & Peters, H. (1968). Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17, 555–7.CrossRefGoogle ScholarPubMed
Petro, E.M., Covaci, A., Leroy, J.L., Dirtu, A.C., De Coen, W. & Bols, P.E. (2010). Occurrence of endocrine disrupting compounds in tissues and body fluids of Belgian dairy cows and its implications for the use of the cow as a model to study endocrine disruption. Sci. Total Environ. 408, 5423–8.CrossRefGoogle Scholar
Rajakoski, E. (1960). The ovarian follicular system in sexually mature heifers with special reference to seasonal, cyclical, end left-right variations. Acta Endocrinol. Suppl. (Copenh.) 34 (Suppl 52), 1–68.Google Scholar
Rodgers, R.J. & Irving-Rodgers, H.F. (2010). Morphological classification of bovine ovarian follicles. Reproduction 139, 309–18.CrossRefGoogle ScholarPubMed
Roy, S.K. & Greenwald, G.S. (1985). An enzymatic method for dissociation of intact follicles from the hamster ovary: histological and quantitative aspects. Biol. Reprod. 32, 203–15.CrossRefGoogle ScholarPubMed
Roy, S.K. & Greenwald, G.S. (1996). Methods of separation and in-vitro culture of pre-antral follicles from mammalian ovaries. Hum. Reprod. Update 2, 236–45.CrossRefGoogle ScholarPubMed
Silva, R.C., Bao, S.N., Jivago, J.L. & Lucci, C.M. (2011). Ultrastructural characterization of porcine oocytes and adjacent follicular cells during follicle development: lipid component evolution. Theriogenology 76, 1647–57.CrossRefGoogle ScholarPubMed
Torrance, C., Telfer, E. & Gosden, R.G. (1989). Quantitative study of the development of isolated mouse pre-antral follicles in collagen gel culture. J. Reprod. Fertil. 87, 367–74.CrossRefGoogle ScholarPubMed
Turnbull, K.E., Braden, A.W. & Mattner, P.E. (1977). The pattern of follicular growth and atresia in the ovine ovary. Aust. J. Biol. Sci. 30, 229–41.CrossRefGoogle ScholarPubMed
van Wezel, I.L. & Rodgers, R.J. (1996). Morphological characterization of bovine primordial follicles and their environment in vivo. Biol. Reprod. 55, 1003–11.CrossRefGoogle ScholarPubMed
Xu, M., West-Farrell, E.R., Stouffer, R.L., Shea, L.D., Woodruff, T.K. & Zelinski, M.B. (2009). Encapsulated three-dimensional culture supports development of nonhuman primate secondary follicles. Biol. Reprod. 81, 587–94.CrossRefGoogle ScholarPubMed
Yu, S.J., Yong, Y. H. & Cui, Y. (2010). Oocyte morphology from primordial to early tertiary follicles of yak. Reprod. Domest. Anim. 45, 779–85.Google ScholarPubMed